Exposure to Cyantraniliprole Adversely Impacts Fitness of Harmonia axyridis: Acute Toxicity and Sublethal Effects on Development, Fecundity and Antioxidant Responses

Abstract

Extensive utilization of pesticides and their persistent residues inadvertently pose threats to the effectiveness and fitness of biocontrol agents in agroecosystems. However, these ecological consequences are generally disregarded when executing integrated pest management strategies (IPM). Cyantraniliprole (CNAP) serves as a wide-spectrum diamide insecticide and its sublethal effects have been well characterized on multiple insect pests, whereas its impacts on beneficial natural enemies remain unfathomed. Herein we exposed Harmonia axyridis, a predacious generalist, to lethal and sublethal concentrations of CNAP via dipping treatment (egg stage) and topical applications (1st-instar stage + adult stage). The acute toxicity tests revealed that LC₅₀ of CNAP were 90.11, 86.11 and 240.50 mg/L against embryos, 1st instar nymphs and female adults, respectively, with safety factors ranging from 1.14 to 5.34, suggesting its medium toxicity for H. axyridis and larval stage was the most susceptible. The embryonic, larval and pupal durations of coccinellids ecdysed from CNAP-treated eggs and 1st instars were all elongated under sublethal concentrations, of which LC₃₀ triggered more pronounced and significant retardations relative to control. Besides, exposed coccinellids displayed substantially diminished pupal mass and pupation rate, most notably for insects molted from the 1st-instar stage upon CNAP sublethal treatments. With respect to reproductive performance, LC₁₀ and LC₃₀ of CNAP all significantly suppressed female fecundity, as evidenced by reduced vitellin content, a prolonged pre-oviposition period (POP), mitigated laid eggs and the egg hatching rate. Specifically, there existed positive correlations between vitellin level (Vn) and number of eggs deposited by per female, indicative of CNAP affecting fecundity by regulation of Vn. In addition, the antioxidant system was also profoundly disrupted by CNAP, with compromised POD activity at different concentrations over time and induced hormesis of SOD/CAT activities post LC₁₀ exposure. Activities of SOD and TAC were enhanced to exert protective functions during the first 48 h, while defense collapsed at 72 h following LC₃₀ treatments that depleted all enzymatic activities. We speculated that fitness trade-offs may occur between reproductive capacity and antioxidant defenses to sustain physiological homeostasis in response to CNAP stress. Collectively, this study evaluated the ecological risk of CNAP and unmasked its adverse implications for overall fitness of H. axyridis, which highlighted rational application of agrochemicals to conserve biocontrol agents when implementing IPM strategies for sustainable pest control.

Keywords: Harmonia axyridis; antioxidant enzymes; cyantraniliprole; development and fecundity; sublethal effects.

Figure 1

Toxic effects of CNAP exposure on development of H. axyridis at immature stages. (A) Embryonic, larval and pupal durations upon sublethal treatments at egg stage. (B) Durations of larvae and pupae grown from 1st instar subjected to sublethal treatments. (C) Fresh weight and (D) pupation rate of insects pupated from embryos and 1st instar treated by CNAP. Each histogram and error bar represented mean ± SEM. Different lowercase letters within the same panel denoted significant differences among groups (p < 0.05).

Figure 2

Effects of CNAP application on reproductive capacity of females within 14 days from the onset of oviposition. Scatter dots were expressed as mean ± SEM (n = 10). Different lowercase letters within each column denoted significant differences among groups on the same day (p < 0.05).

Figure 3

Toxic effects on POP and egg hatching rate (A) as well as vitellin level (72 h after exposure) (B) of females treated by CNAP. Red lines and green/purple triangles denoted means and specific values, while boundaries of boxes signified the 25/75th percentiles and whiskers indicated minimum/maximum, with horizontal lines as medians. Histograms plus error bars represented mean ± SEM. Different letters above marked significant differences among groups (p < 0.05).

Figure 4

Pearson correlation analysis between vitellin level (72 h) and number of eggs laid by individual female at day 7 since oviposition. The minimum, median, and maximum values of each group (Figure 2, day 7) were aligned with the vitellin abundance (Figure 3B) accordingly.

Figure 5

TAC (A), SOD (B), CAT (C) and POD (D) activity in females amenable to sublethal exposure of CNAP at 24, 48 and 72 h. Each histogram indicated the mean of three repetitions (n = 3) and error bars depicted SEM. Different lowercase letters denoted statistically significant differences among groups (p < 0.05).